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    大黃屬(蓼科)植物ndhF基因的適應(yīng)性進化

    2016-03-21 05:54:35李景劍劉合霞毛世忠黃仕訓
    廣西植物 2016年1期

    李景劍,劉合霞,毛世忠,趙 博,3,黃仕訓*

    ( 1.華南農(nóng)業(yè)大學林學與風景園林學院,廣州510642; 2.廣西壯族自治區(qū)廣西植物研究所,中國科學院廣西桂林541006; 3.中國中醫(yī)科學院中藥研究所,北京100700 )

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    大黃屬(蓼科)植物ndhF基因的適應(yīng)性進化

    李景劍1,2,劉合霞2,毛世忠2,趙博2,3,黃仕訓2*

    ( 1.華南農(nóng)業(yè)大學林學與風景園林學院,廣州510642; 2.廣西壯族自治區(qū)廣西植物研究所,
    中國科學院廣西桂林541006; 3.中國中醫(yī)科學院中藥研究所,北京100700 )

    摘要:大黃屬( Rheum L.)是蓼科( Polygonaceae)中一個高度分化的大屬,廣泛分布在亞洲和歐洲的高山和沙漠地區(qū),全世界約60種,其中在青藏高原及其鄰近地區(qū)發(fā)現(xiàn)了約40種。該屬種的高度分化曾被推測是第三紀末青藏高原的快速隆升以及第四紀氣候的反復變化所引發(fā)的適應(yīng)性輻射導致。為進一步了解大黃屬植物輻射式物種分化的分子適應(yīng)機制,該研究選取34個形態(tài)上多樣化的大黃屬物種,利用系統(tǒng)發(fā)育分析軟件,在時間框架下采用位點模型和分支模型對大黃屬的葉綠體ndhF基因進行了適應(yīng)性進化分析。結(jié)果表明:大黃屬植物的分

    李景劍,劉合霞,毛世忠,等.大黃屬(蓼科)植物ndhF基因的適應(yīng)性進化[J].廣西植物,2016,36( 1) : 101-106

    LI JJ,LIU HX,MAO SZ,et al.Adaptive evolution of the ndhF gene in the genus Rheum ( Polygonaceae)[J].Guihaia,2016,36( 1) : 101-106

    關(guān)鍵詞:大黃屬(蓼科),ndhF基因,分支模型,位點模型,正選擇位點

    The genus Rheum ( Polygonaceae) with about 60 species,primarily distributed in mountainous and desert regions of the Qinghai-Tibetan Plateau and adjacent areas ( Kao&Cheng,1975; Li,1998).The distribution and the ancestral area reconstruction analyses consistently suggested that rapid radiations of Rheum have occurred,and may have been caused by the extensive uplifts of the Qinghai-Tibetan Plateau ( Wang et al,2005; Wan et al,2011; Sun et al,2012).To adapt to the new alterations of habitat,morphological traits of this genus are highly diversified.Some species have evolved into dwarf plants with coriaceous basal leaves or drooping bracts to defense them from freeze injury and could distribute up to snow line at altitude of 5 400 m,for example R.Nobile ( Xie,2000).For other species,stem leaves are have degenerated and basal leaves are covered with verruca or indumentum to reduce water transpiration,to avoid the burning from high temperature and to avoid damage by strong winds,therefore,these species can grow in the Gobi Desert at altitude 700 m.R.palaestinum in particular,has broad,rigid leaves,with a waxy surface,and channels cut into them that funnel any water that drops onto them toward its root,with enough force to cause deep soil penetration ( Lev-Yadun et al,2009).These changes in morphology and physiology might be resulted from the adaptive evolution of some genes which encode functional proteins,such as chloroplast ndhF gene that related to photosynthesis and photorespiration ( Zapata et al,2005).

    Chloroplast is thought to be a very conservative part of plant genome but little is known about the evolution of this plastome promoters.Previous study showed that the alignment of sequences upstream ndhF suggested that promoters of this gene underwent comparatively rapid evolution in flowering plants ( Seliverstov et al,2009).The ndhF gene is located in a small single-copy region of the chloroplast genome that rarely underwent substantial rearrangements in terrestrial plants ( Hiratsuka et al,1989).Its nucleotide sequence predicts a hydrophobic protein of 664 amino acids with a calculated mass of 72.9 kDa ( Schluchter et al,1993).The ndhF gene encodes NADH dehydrogenase F subunit of the plastid NDH complex which regulated the activity of NDH complexes by its phosphorylation.The plastid NDH complex in chloroplast thylakoid membranes is involved in photosystem I cyclic and chlororespiratory electron transport in photosynthetic regulation of higher plants ( Lascano et al,2003).

    Considering the adaptability of Rheum to extreme habitats,the sequences of ndhF gene from 34 species of Rheum and 2 species of Oxyria in Polygonaceae were retrieved from the National Center for Biotechnology Information ( NCBI) for adaptive evolution testing in this study.Our finding may provide new molecular evidence for the rapid putative radiations of Rheum triggered by the recent uplifts of the Qinghai-Tibetan Plateau.

    1 Materials and Methods

    Thirty-four species of Rheum and two species of Oxyria in Polygonaceae used in this study were listed in Table 1.Sequences of ndhF gene were downloaded from NCBI ( http: / /www.ncbi.nlm.nih.gov/guide/).Sequence alignments were conducted using the software CLUSTAL W ver.1.83 ( Thompson et al,1994) and adjusted manually in BioEdit 5.0.9.1 ( Hall,1999).Oxyria digyna and O.sinensis were used as outgroup.Maximum Parsimony ( MP) analysis was conducted using PAUP 4.0b10 ( Swofford,2003),Heuristic searches were conducted 1 000 times with random taxon-addition sequences,with tree-bisection-reconnection ( TBR) branch swapping,and with the options MULPARS in effect and STEEPEST DE-SCENT off.Support for internal nodes was estimated with bootstrap values ( Felsenstein,1985).

    Table 1 Species names and accession numbers of ndhF sequences

    Based on the MP tree,the analysis of adaptive evolution of ndhF gene was implemented in the program of CODEML from PAML package version 4 ( Yang,2007).The lnL values under one-ratio model as well as free ratio model were calculated,and the Likelihood Ratio Test ( LRT) was conducted to test whether there were different ratios for each lineage.Site-specific models,which allowed the ω ratio to vary among sites but fixed a single ω ratio in all branches,were used to detect positive selection and to identify positively selected sites.Three pairs of site-specific models were calculated to test for recurrent,diversifying,selection: M0 ( one ratio) and M3 ( Discrete),M1 ( Neutral) and M2 ( Selection),and M7 ( Beta) and M8 ( Beta&ω).( Yang&Nielsen,2002; Yang et al,2005).Log likelihoods of models ( M1 vs.M2; M0 vs.M3; M7 vs.M8) were compared using LRT.

    For the spatial analysis of the codon site under positive selection,the PSIPRED server ( http: / /bioinf.cs.ucl.a(chǎn)c.uk/psipred/) was used to analysis the secondary structure of NDHF subunit for Rheum palaestinum.

    2 Results and Analysis

    The ndhF dataset had an aligned length of 1 944 characters in the dataset,of which,1 751 characters were constant,111 were variable and parsimony-uninformative,and 82 were parsimony-informative.Maximum Parsimony analysis yielded 84 equally parsimonious trees,and a strict consensus tree of these trees was shown in Fig.1.The topology of MP tree was consistent with the molecular phylogenies published to date ( Wang et al,2005; Sun et al,2012).The consensus tree revealed three major clades ( A,B,C) within the genus Rheum,all species of Rheum comprised a well-supported lineage,with a sister relationship to Oxyria.

    To analyze the possibility that positive selection acts on ndhF genes,we used the maximum-likelihood codon model from the CODEML program in the PAML4 package.The topology of the MP tree mentioned above was modified for all CODEML analyses.All calculations and tests are listed in Tables 2 and 3.Under the one-ratio model which allowed for only a single ω ratio across all sites of the gene phylogeny and the same ω ratio for all branches in the phylogenic tree ( Fig.1),the loglikelihood value was ω= 0.296 5,lower than 1 ( Table 2).In the branch-specific analysis,the LRT statistic for the comparison of the one-ratio model vs.the free-ratio model was 2Δ=77.467 0 with P<0.05 and df=54,suggesting that there had different ratios for each lineage of Rheum species ( Table 3).But no sites with a Bayesian posterior probability of positive selection larger than 0.95 in one or more cases were found when analyzed by Bayes.

    In site-specific models,models M2,M3 and M8 allowed sites with ω>1.The LRT statistic of M0-M3,M1-M2 and M7-M8 comparison all with P<0.05,so models M3,M2 and M8 was significantly better than M0,M1 and M7.Under both M2 and M8 models,three sites were under positive selection with ω>1 and identified three NDHF residues ( 188H,465H,551L) with a Bayesian posterior probability of positive selection larger than 0.95 in one or more cases when analyzed by Empirical Bayes ( Table 2).

    Fig.1 Strict consensus tree from maximum-parsimony ( MP) analysis based on ndhF sequences of Rheum Numbers above the branches indicate bootstrap values by MP analysis.Numbers with bootstrap values>50% are shown.Shadows on the right indicatefive clades of Rheum displaying rapid radiation.

    With no obvious sequence similarity to structures present in PDB,the secondary structure of NDHF subunit for Rheum palaestinum was predicted by PSIPRED server ( Fig.2).The test results showed the 188th amino acid which located in the α-helix was histidine ( H) in R.palaestinum,while asparagine ( N) was also found in other species of Rheum.The amino acid encoded by the 465th codon was histidine ( H) in R.palaestinum,while asparagine ( N) and tyrosine ( Y) was found in other species of Rheum.In addition,the 551th codon encoded was leucine ( L) in R.palaestinum,while phenylalanine ( F) was found in other species of Rheum.

    3 Discussion

    The distribution and the ancestral area reconstruction analyses suggests that rapid putative radiations of Rheum might have been triggered by the recent uplifts of the Qinghai-Tibetan Plateau and the Quaternary climate oscillations.Geological evidence indicates that at least four different periods at the early Miocene ( i.e.,22,15 -13,8-7,and 3.5-1.6 Ma) occurred during recent extensive uplifting of the Qinghai-Tibetan Plateau ( Shi et al,1998; Sun et al,2012),and new habitats may have been created while old ones became fragmented within each period.The new alterations of habitat of Rheum species are various,from snow line at altitude 5 400 m to Gobi Desert at altitude 700 m.Through the adaptive evolution of ndhF gene involved in photosynthesis pathways,some species of Rheum could adapt the extreme habitats.

    By comparing Models M1a/M2a and M7/M8,threeamino acid sites ( 188H,465H,551L) were identified under positive selection.The secondary structure of NDHF subunit showed thatthe positively selected sites ( 465H and 551L) were on the loops.The 188th amino acid which located in the α-helix was histidine ( H) in R.palaestinum ( Fig.2),while asparagine ( N) was found in other species.The ndhF gene encoded a subunit of the plastid NDH complex,and this complex assembly might be regulated on the pos-transcriptional level in a way that the quantity of whole NDH complexescould be determined by the quantity of one of its subunits,e.g.NDHF.The activity of NDH complexes was also regulated by phosphorylation of the NDHF polypeptide.Our study found that the ndhF gene was at high expression level under stress conditions,and those stress factors from environment might be the selective pressure to lead the adaptive evolution of ndhF gene.Our results indicated that the change of spatial structure may have a relationship with the adaptation of Rheum to the environment.For example,R.palaestinum with histidine mutation on the 188th codon site is the rare Rheum plant growing in mountainous desert areas ( receiving an average annual rainfall of ca.75 mm) in the world,and it has a single deep main vertical root ( Zohary,1966).Previous studies released that histidine is one of the essential amino acids for plant growth and survival,especially for root meristem maintenance,the higher histidine content in plant,the faster root growth and better adaptability to the environments ( Mo,2006; Malki&Jaeobs,2001).So the adaptive evolution of ndhF subunit might be important for Rheum species to adapt various habitats.

    Table 2 Maximum likelihood parameter estimates for ndhF gene

    Fig.2 The secondary structures of NDHF protein for Rheum palaestinum The sites ( 188H,465H,551L) under adaptive evolution are marked with red boxes.

    Table 3 Likelihood ratio test ( LRTs) of the variable ω ratios under different models for ndhF gene

    AcknowledgementsWe are grateful to LIU Lei for his help with data analysis and Qian Guo for language editing support.

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    *通訊作者:黃仕訓,研究員,主要從事瀕危植物保護研究,( E-mail) hsx@ gxib.cn。book=102,ebook=107子進化系統(tǒng)樹呈現(xiàn)短而平行的輻射式分支式樣,顯示出典型的物種快速輻射多樣化特征;用位點模型檢驗ndhF基因是否存在經(jīng)受正向選擇(ω>1)時,在氨基酸水平上共鑒定出3個NDHF亞基的正選擇位點( 188H,465H,551L),對NDHF亞基的二級結(jié)構(gòu)進行分析后發(fā)現(xiàn)編碼的188H氨基酸位于α螺旋上。大黃屬植物可能通過這些結(jié)構(gòu)域的適應(yīng)性進化,適應(yīng)青藏高原的快速隆升以及第四紀氣候的反復變化而引發(fā)的陸地生態(tài)系統(tǒng)改變。該研究結(jié)果可為今后對該屬植物的實驗分析提供首選位點。

    作者簡介:李景劍( 1983-),男,廣東廉江人,博士研究生,主要從事植物分子生物學研究,( E-mail) calljone@163.com。

    基金項目:國家科技基礎(chǔ)性工作專項( 2009FY120200) ;廣西自然科學基金( 2012GXNSFBA053075) ;廣西植物研究所基本業(yè)務(wù)費(桂植業(yè)14003) [Supported by the Special Program for Basic Research of Science and Technology of China( 2009FY120200) ; the Natural Science Foundation of Guangxi ( 2012GXNSFBA053075) ; the Science Research Foundation of Guangxi Institute of Botany ( Guizhiye14003)]。

    收稿日期:2015-08-24修回日期: 2015-12-02

    DOI:10.11931/guihaia.gxzw201508017

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